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REVIEW

Ruminant glycogen metabolism

G. E. Gardner A B , P. McGilchrist A and D. W. Pethick A
+ Author Affiliations
- Author Affiliations

A School of Veterinary and Life Science, Murdoch University, Murdoch, WA 6150, Australia.

B Corresponding author. Email: G.Gardner@murdoch.edu.au

Animal Production Science 54(10) 1575-1583 https://doi.org/10.1071/AN14434
Submitted: 24 March 2014  Accepted: 30 June 2014   Published: 19 August 2014

Abstract

The biochemistry of glycogen metabolism is well characterised, having been extensively studied in laboratory rodents and humans, and from this stems the bulk of our knowledge regarding the metabolism of glycogen in ruminants. With respect to intermediary metabolism, the key tissues include the liver and muscle. The liver glycogen depot plays a central role in intermediary metabolism, storing and mobilising glycogen during the fed and fasted metabolic states, with these responses modulated during pregnancy, lactation, and exercise. Alternatively, the muscle glycogen depot is particularly important for local energy homeostasis, and is likely to be less important as a key post-prandial sink for blood glucose given the reduced absorption of glucose from the gut in ruminant animals. Yet similar to the liver, this depot is also in a constant state of turnover, with the muscle glycogen concentration at any point in time a reflection of the rates of glycogen synthesis and degradation. Muscle glycogen metabolism attracts particular attention given its importance for post-mortem acidification of muscle tissue, with a shortage at slaughter leading to dark cutting meat. Simplistically the concentration of muscle glycogen at slaughter is a function of two key factors, the on-farm starting levels of glycogen minus the amount depleted during the pre-slaughter phase. On-farm concentrations of muscle glycogen are largely a reflection of metabolisable energy intake driving increased rates of muscle glycogen synthesis. Compared with simple-stomached species the rate of glycogen synthesis within ruminants is relatively low. Yet there also appears to be differences between sheep and cattle when fed diets of similar metabolisable energy, with cattle repleting muscle glycogen more slowly after depletion through exercise. While metabolisable energy intake is the key driver, genetic and age-related factors have also been shown to influence glycogen repletion. The amount of muscle glycogen depleted during the pre-slaughter phase is largely associated with stress and adrenaline release, and several recent studies have characterised the importance of factors such as exercise, age and genetics which modulate this stress response. This paper presents a summary of recent experiments in both cattle and sheep that highlight current developments in the understanding of this trait.

Additional keywords: adrenalin, energy-intake, insulin, muscle liver.


References

Ballard FJ, Hanson RW, Kronfeld DS (1969) Gluconeogenesis and lipogenesis in tissue from ruminant and nonruminant animals. Federation Proceedings 28, 218–231.

Bassett JM (1972) Plasma glucagon concentrations in sheep: their regulation and relation to concentrations of insulin and growth hormone. Australian Journal of Biological Sciences 25, 1277–1287.

Bell AW, Gardner JW, Manson W, Thompson GE (1975) Acute cold exposure and the metabolism of blood glucose, lactate and pyruvate, and plasma amino acids in the hind leg of the fed and fasted young ox. The British Journal of Nutrition 33, 207–217.
Acute cold exposure and the metabolism of blood glucose, lactate and pyruvate, and plasma amino acids in the hind leg of the fed and fasted young ox.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXhtV2lu7w%3D&md5=c64b0d66bbe2d051569865b5479174c1CAS | 1115760PubMed |

Brandstetter AM, Picard B, Geay Y (1998) Muscle fibre characteristics in four muscles of growing bulls. I. Postnatal differentiation. Livestock Production Science 53, 15–23.
Muscle fibre characteristics in four muscles of growing bulls. I. Postnatal differentiation.Crossref | GoogleScholarGoogle Scholar |

Briand M, Talmant A, Braind Y, Monin G, Durand R (1981) Metabolic types of muscle in sheep: I. Myosin ATPase, glycolytic, and mitochondrial enzyme activities. European Journal of Applied Physiology 46, 347–358.
Metabolic types of muscle in sheep: I. Myosin ATPase, glycolytic, and mitochondrial enzyme activities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXlvVCntL8%3D&md5=4d3344e60cb0f900b2956a35874bd5c4CAS |

Brockman RP, Laarveld B (1986) Hormonal-regulation of metabolism in ruminants – a review. Livestock Production Science 14, 313–334.
Hormonal-regulation of metabolism in ruminants – a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XkvFWnsLc%3D&md5=6c49e8dcfb716fbb9efc9fce3e79e043CAS |

Burdick NC, Carroll JA, Hulbert LE, Dailey JW, Willard ST, Vann RC, Welsh TH, Randel RD (2010) Relationships between temperament and transportation with rectal temperature and serum concentrations of cortisol and epinephrine in bulls. Livestock Science 129, 166–172.
Relationships between temperament and transportation with rectal temperature and serum concentrations of cortisol and epinephrine in bulls.Crossref | GoogleScholarGoogle Scholar |

Burdick NC, Carroll JA, Hulbert LE, Dailey JW, Ballou MA, Randel RD, Willard ST, Vann RC, Welsh TH (2011) Temperament influences endotoxin-induced changes in rectal temperature, sickness behavior, and plasma epinephrine concentrations in bulls. Innate Immunity 17, 355–364.
Temperament influences endotoxin-induced changes in rectal temperature, sickness behavior, and plasma epinephrine concentrations in bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGisrvK&md5=48bdc6597619b42dd5ae7bf3fa6cf2dcCAS | 20682590PubMed |

Cafe LM, Robinson DL, Ferguson DM, McIntyre BL, Geesink GH, Greenwood PL (2011) Cattle temperament: persistence of assessments and associations with productivity, efficiency, carcass and meat quality traits. Journal of Animal Science 89, 1452–1465.
Cattle temperament: persistence of assessments and associations with productivity, efficiency, carcass and meat quality traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXls1Oiu74%3D&md5=428fb5ad67bc4579d593e39d0492fae8CAS | 21169516PubMed |

Coombes SV, Gardner GE, Pethick DW, McGilchrist P (2014) The impact of animal temperament on muscle glycogen, muscle lactate and plasma lactate concentrations at slaughter. Meat Science in press.

Curley KO, Carroll JA, Vann RC, Randel RD, Welsh TH (2010) Comparison of adrenal responsiveness to corticotropin-releasing hormone (CRH) in Angus and Brahman steers of divergent temperament. Journal of Dairy Science 93, 19

Daly BL, Gardner GE, Ferguson DM, Thompson JM (2006) The effect of time off feed prior to slaughter on muscle glycogen metabolism and rate of pH decline. Australian Journal of Agricultural Research 57, 1229–1235.
The effect of time off feed prior to slaughter on muscle glycogen metabolism and rate of pH decline.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFeqsr7M&md5=78d7e290ba25ed0f23be96aea41ed49bCAS |

Davidovich A, Bartley EE, Chapman TE, Bechtle RM, Dayton AD, Frey RA (1977) Ammonia toxicity in cattle. II. Changes in carotid and jugular blood components associated with toxicity. Journal of Animal Science 44, 702–709.

Ebner K, Wotjak CT, Landgraf R, Engelmann M (2005) Neuroendocrine and behavioral response to social confrontation: residents versus intruders, active versus passive coping styles. Hormones and Behavior 47, 14–21.
Neuroendocrine and behavioral response to social confrontation: residents versus intruders, active versus passive coping styles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVaqt73O&md5=3dc2ca1f66b7146848281647599034f5CAS | 15579261PubMed |

Felig P, Wahren J, Hendler R (1975) Influence of oral glucose ingestion on splanchnic glucose and gluconeogenic substrate metabolism in man. Diabetes 24, 468–475.
Influence of oral glucose ingestion on splanchnic glucose and gluconeogenic substrate metabolism in man.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXkvFCnu74%3D&md5=a5e8dfe30bb511190413bb3923689156CAS | 1126590PubMed |

Ferguson DM, Bruce HL, Thompson JM, Egan AF, Perry D, Shorthose WR (2001) Factors affecting beef palatability – farmgate to chilled carcass. Australian Journal of Experimental Agriculture 41, 879–891.
Factors affecting beef palatability – farmgate to chilled carcass.Crossref | GoogleScholarGoogle Scholar |

Fernandez JM, Croom WJ, Johnson AD, Jaquette RD, Edens FW (1988) Subclinical ammonia toxicity in steers: effects on blood metabolite and regulatory hormone concentrations. Journal of Animal Science 66, 3259–3266.

Franch J, Aslesen R, Jensen J (1999) Regulation of glycogen synthesis in rat skeletal muscle after glycogen-depleting contractile activity: effects of adrenaline on glycogen synthesis and activation of glycogen synthase and glycogen phosphorylase. Journal of Biochemistry 344, 231–235.
Regulation of glycogen synthesis in rat skeletal muscle after glycogen-depleting contractile activity: effects of adrenaline on glycogen synthesis and activation of glycogen synthase and glycogen phosphorylase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns1yjtL0%3D&md5=2450917806adb5fc32cc793eafd2c53dCAS |

Gardner GE, Kennedy L, Milton JTB, Pethick DW (1999) Glycogen metabolism and ultimate pH of muscle in Merino, first-cross, and second-cross wether lambs as affected by stress before slaughter. Australian Journal of Agricultural Research 50, 175–181.
Glycogen metabolism and ultimate pH of muscle in Merino, first-cross, and second-cross wether lambs as affected by stress before slaughter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhslCrs7s%3D&md5=acb7351768acf5b8f8c94566bdb0161fCAS |

Gardner GE, Jacobs RH, Pethick DW (2001a) The effect of magnesium oxide supplementation on muscle glycogen metabolism before and after exercise and at slaughter in sheep. Australian Journal of Agricultural Research 52, 723–729.
The effect of magnesium oxide supplementation on muscle glycogen metabolism before and after exercise and at slaughter in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvVCrsLo%3D&md5=0a21a1ae3735fa5f530f7108a76fb380CAS |

Gardner GE, McIntyre BL, Tudor G, Pethick DW (2001b) The impact of nutrition on bovine muscle glycogen metabolism following exercise. Australian Journal of Agricultural Research 52, 461–470.
The impact of nutrition on bovine muscle glycogen metabolism following exercise.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFShsrY%3D&md5=fca8f6b85d561f0462ae8f5f4209a685CAS |

Gardner GE, McIntyre BL, Tudor GD, Pethick DW (2001c) Nutritional influences on muscle glycogen recovery following exercise in sheep and cattle. In ‘Recent advances in animal nutrition in Australia’. (Ed. JL Corbett) pp. 145–52. (The University of New England: Armidale, NSW)

Gardner GE, McGilchrist P, Thompson JM, Martin KM (2009) Selection for muscling reduces muscle response to adrenaline. In ‘International symposium of ruminant physiology’. (Eds Y Chilliard, F Glasser, Y Faulconnier, F Bocquier, I Veissier, M Doreau) pp. 430–431. (Wageningen Academic Publishers: Clermont Ferrand, France)

Gardner GE, McIntyre BL, Tudor GD, Pethick DW (2013) Diets high in rumen degradable nitrogen reduce bovine muscle glycogen concentration at slaughter. In ‘59th international congress of meat science and technology’. (Eds M Serdaroglu, B Ozturk, T Akcan) (E-Book Proceedings: Izmir, Turkey)

Goodyear LJ, Hirshman MF, Smith RJ, Horton ES (1991) Glucose transporter number, activity, and isoform content in plasma membranes of red and white skeletal muscle. The American Journal of Physiology 261, E556–E561.

Greenwood PL, Gardner GE, Hegarty RS (2006) Lamb myofibre characteristics are influenced by sire estimated breeding values and pastoral nutritional system. Australian Journal of Agricultural Research 57, 627–639.
Lamb myofibre characteristics are influenced by sire estimated breeding values and pastoral nutritional system.Crossref | GoogleScholarGoogle Scholar |

Gruber SL, Tatum JD, Engle TE, Chapman PL, Belk KE, Smith GC (2010) Relationships of behavioral and physiological symptoms of preslaughter stress to beef longissimus muscle tenderness. Journal of Animal Science 88, 1148–1159.
Relationships of behavioral and physiological symptoms of preslaughter stress to beef longissimus muscle tenderness.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktVyjs7w%3D&md5=cdcb1baf13b10efcc65e7b768b0b9257CAS | 19897634PubMed |

Gunja-Smith Z, Marshall JJ, Mercier C, Smith EE, Whelan WJ (1970) A revision of the Meyer–Bernfeld model of glycogen and amylopectin. FEBS Letters 12, 101–104.
A revision of the Meyer–Bernfeld model of glycogen and amylopectin.Crossref | GoogleScholarGoogle Scholar | 11945551PubMed |

Haman F, Peronnet F, Kenny GP, Massicotte D, Lavoie C, Weber JM (2005) Partitioning oxidative fuels during cold exposure in humans: muscle glycogen becomes dominant as shivering intensifies. The Journal of Physiology 566, 247–256.
Partitioning oxidative fuels during cold exposure in humans: muscle glycogen becomes dominant as shivering intensifies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvVyqsbw%3D&md5=0a007fbdbe0e49b10a550718dca98fceCAS | 15831534PubMed |

Holness MJ, MacLennan PA, Palmer TN, Sugden MC (1988) The disposition of carbohydrate between glycogenesis, lipogenesis and oxidation in liver during the starved-to-fed transition. Biochem Journal 252, 325–330.

Jacob RH, Pethick DW, Chapman HM (2005) Muscle glycogen concentrations in commercial consignments of Australian lamb measured on farm and post-slaughter after three different lairage periods. Australian Journal of Experimental Agriculture 45, 543–552.
Muscle glycogen concentrations in commercial consignments of Australian lamb measured on farm and post-slaughter after three different lairage periods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFOmtbc%3D&md5=86c15fc40d04e9464b58aaf90cca762aCAS |

Jacob RH, Gardner GE, Pethick DW (2009) Repletion of glycogen in muscle is preceded by repletion of glycogen in the liver of Merino hoggets. Animal Production Science 49, 131–138.
Repletion of glycogen in muscle is preceded by repletion of glycogen in the liver of Merino hoggets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVehsb4%3D&md5=211faabdf3b2e332662053633d32dce9CAS |

Johnson RR (1976) Influence of carbohydrate solubility on non-protein nitrogen utilization in the ruminant. Journal of Animal Science 43, 184–191.

Kay RN (1983) Rumen function and physiology. The Veterinary Record 113, 6–9.
Rumen function and physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXkvVGmtr8%3D&md5=958b652018c92870ecbc45fe6556adaeCAS | 6880003PubMed |

Knee BW, Cummins LJ, Walker P, Warner R (2004) Seasonal variation in muscle glycogen in beef steers. Australian Journal of Experimental Agriculture 44, 729–734.
Seasonal variation in muscle glycogen in beef steers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslShurg%3D&md5=6d31d9cd66e7f13a5b92e37e7e05b083CAS |

Knee BW, Cummins LJ, Walker PJ, Kearney GA, Warner RD (2007) Reducing dark-cutting in pasture-fed beef steers by high-energy supplementation. Australian Journal of Experimental Agriculture 47, 1277–1283.
Reducing dark-cutting in pasture-fed beef steers by high-energy supplementation.Crossref | GoogleScholarGoogle Scholar |

Kumar R (1998) ‘Expression of glycogenin in ovine muscle under differing metabolic conditions.’ (School of Veterinary and Biomedical Science, Murdoch University: Murdoch, WA)

Maehlum S, Felig P, Wahren J (1978) Splanchnic glucose and muscle glycogen metabolism after glucose feeding during postexercise recovery. The American Journal of Physiology 235, E255–E260.

Martin WH, Murphree SS, Saffitz JE (1989) Beta-adrenergic receptor distribution among muscle fiber types and resistance arterioles of white, red, and intermediate skeletal muscle. Circulation Research 64, 1096–1105.
Beta-adrenergic receptor distribution among muscle fiber types and resistance arterioles of white, red, and intermediate skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXksFSqsb4%3D&md5=c0a6f243b41c336f798189d498a8e9c9CAS | 2541942PubMed |

Martin KM, Gardner GE, Thompson JM, Hopkins DL (2004) Nutritional impact on muscle glycogen metabolism in lambs selected for muscling. Journal of Animal and Feed Sciences 13, 639–642.

Martin KM, McGilchrist P, Thompson JM, Gardner GE (2011) Progeny of high muscling sires have reduced muscle response to adrenaline in sheep. Animal 5, 1060–1070.
Progeny of high muscling sires have reduced muscle response to adrenaline in sheep.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38vovV2isQ%3D%3D&md5=9654afb82fccc89b714ac9ffe8314742CAS | 22440101PubMed |

McGilchrist P (2011) ‘Selection for muscling effects carbohydrate and fatty acid metabolism in beef cattle.’ (School of Veterinary and Biomedical Sciences, Murdoch University: Murdoch, WA)

McGilchrist P, Pethick DW, Bonny SPF, Greenwood PL, Gardner GE (2011a) Beef cattle selected for increased muscularity have a reduced muscle response and increased adipose tissue response to adrenaline. Animal 5, 875–884.
Beef cattle selected for increased muscularity have a reduced muscle response and increased adipose tissue response to adrenaline.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38vovVyktg%3D%3D&md5=86616898e73a3fd2e532db40797de427CAS | 22440027PubMed |

McGilchrist P, Pethick DW, Bonny SPF, Greenwood PL, Gardner GE (2011b) Whole body insulin responsiveness is higher in beef steers selected for increased muscling. animal 5, 1579–1586.
Whole body insulin responsiveness is higher in beef steers selected for increased muscling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1yms7rI&md5=d967b79e694e911793b7d5919dc63dedCAS | 22440349PubMed |

McGilchrist P, Alston CL, Gardner GE, Thomson KL, Pethick DW (2012) Beef carcasses with larger eye muscle areas, lower ossification scores and improved nutrition have a lower incidence of dark cutting. Meat Science 92, 474–480.
Beef carcasses with larger eye muscle areas, lower ossification scores and improved nutrition have a lower incidence of dark cutting.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38jjsVKhuw%3D%3D&md5=fe9793a8548011feaa3267536b957463CAS | 22717222PubMed |

Meinke MH, Edstrom RD (1991) Muscle glycogenolysis. Regulation of the cyclic interconversion of phosphorylase a and phosphorylase b. The Journal of Biological Chemistry 266, 2259–2266.

Mellgren RL, Coulson M (1983) Coordinated feedback regulation of muscle glycogen metabolism: inhibition of purified phosphorylase phosphatase by glycogen. Biochemical and Biophysical Research Communications 114, 148–154.
Coordinated feedback regulation of muscle glycogen metabolism: inhibition of purified phosphorylase phosphatase by glycogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXks1KmtLk%3D&md5=946ccae40e340850eb74c26757beccc3CAS | 6309163PubMed |

MLA (2013) Meat Standards Australia annual outcomes report 2012–13. In ‘Annual outcomes reports’. (Ed. MLA) Available at http://www.mla.com.au/files/7bd7071d-bf9c-482e-b2e4-a24a0094d090/MSA_AOR12-13_web.pdf [Verified 4 July 2014]

Orskov ER, Ryle M (1990) ‘Energy nutrition in ruminants.’ (Elsevier Applied Science: London)

Pethick DW (1984) Energy metabolism in skeletal muscle. In ‘Ruminant physiology: concepts and consequences’. (Eds SK Baker, JM Gawthorne, JB Mackintosh, DB Purser) pp. 277–287. (University of Western Australia: Perth)

Pethick DW (1993) Carbohydrate and lipid oxidation during exercise. Australian Journal of Agricultural Research 44, 431–441.
Carbohydrate and lipid oxidation during exercise.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltVGit78%3D&md5=0bd322a1d60710a22d674c21b5055fb6CAS |

Pethick DW, Rowe JB (1996) The effect of nutrition and exercise on carcass parameters and the level of glycogen in skeletal muscle of Merino sheep. Australian Journal of Agricultural Research 47, 525–537.
The effect of nutrition and exercise on carcass parameters and the level of glycogen in skeletal muscle of Merino sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XislKgs7k%3D&md5=7fa6e2c694e10290780640fca98930aaCAS |

Pethick DW, Lindsay DB, Barker PJ, Northrop AJ (1983) Metabolism of circulating non-esterified fatty acids by the whole animal, hindlimb, and uterus of pregnant ewes. The British Journal of Nutrition 49, 129–143.
Metabolism of circulating non-esterified fatty acids by the whole animal, hindlimb, and uterus of pregnant ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXks1yju7o%3D&md5=eba1649c892438e3a317aecf04474230CAS | 6821682PubMed |

Pethick DW, Miller CB, Harman NG (1991) Exercise in Merino sheep – the relationship between work intensity, endurance, anaerobic threshold and glucose metabolism. Australian Journal of Agricultural Research 42, 599–620.
Exercise in Merino sheep – the relationship between work intensity, endurance, anaerobic threshold and glucose metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXktVGrurg%3D&md5=acbb7309bea181af71a99c379cdc7a9dCAS |

Pethick DW, Cummins L, Gardner GE, Jacobs RH, Knee BW, McDowell M, McIntyre BL, Tudor G, Walker PJ, Warner RD (2000) The regulation of glycogen level in the muscle of ruminants by nutrition. Proceedings of the New Zealand Society of Animal Production 60, 94–97.

Pethick DW, Harper G, Dunshea FD (2005) Fat metabolism and turnover. In ‘Quantitative aspects of ruminant digestion and metabolism’. (Eds J Dijkstra, JM Forbes, J France) pp. 345–371. (CABI Publishing: Wallingford, UK)

Petterson JA, Dunshea FR, Ehrhardt RA, Bell AW (1993) Pregnancy and undernutrition alter glucose metabolic responses to insulin in sheep. The Journal of Nutrition 123, 1286–1295.

Raggi F, Kronfeld DS, Kleiber M (1960) Glucose-6-phosphatase activity in various sheep tissues. Proceedings of the Society for Experimental Biology and Medicine 105, 485–486.
Glucose-6-phosphatase activity in various sheep tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3MXksVSmsg%3D%3D&md5=7cfa7f56f935dc7aae5ec614c0aad7f9CAS | 13739125PubMed |

Randle PJ, Garland PB, Hales CN, Newsholme EA (1963) The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. Lancet 281, 785–789.
The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus.Crossref | GoogleScholarGoogle Scholar |

Richter E, Galbo H (1986) High glycogen levels enhance glycogen breakdown in isolated contracting skeletal muscle. Journal of Applied Physiology 61, 827–831.

Roach PJ (1990) Control of glycogen synthase by hierarchal protein phosphorylation. The FASEB Journal 4, 2961–2968.

Saltin B, Gollnick PD (1983) Skeletal muscle adaptability: significance for metabolism and performance. In ‘Handbook of physiology, section 10, skeletal muscle’. (Eds LD Peachey, RH Adrian, SR Geiger) pp. 555–631. (American Physiological Society: Bethesda, MD)

Smetana R, Huber K, Hartter E, Yang P, Meisinger V, Konnaris C, Gabriel H, Zehetgruber M, Klappacher G, Spona J, Vierhapper H (1995) Coronary artery disease – magnesium and catecholamine interactions during stress burden. In ‘Advances in magnesium research: magnesium in cardiology’ . (Ed. R Smetana) pp. 61–65. (John Libbey and Company Ltd: London)

Stangassinger M, Geisecke D (1986) Splanchnic metabolism of glucose and related energy substrates. In ‘Control of digestion and metabolism in ruminants’. (Eds LP Milligan, WL Grovum, A Dobson) pp. 347–66. (Prentice-Hall: Englewood Cliffs, NJ)

Symonds HW, Mather DL, Collis KA (1981) The maximum capacity of the liver of the adult dairy cow to metabolize ammonia. The British Journal of Nutrition 46, 481–486.
The maximum capacity of the liver of the adult dairy cow to metabolize ammonia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XotlagtQ%3D%3D&md5=c1f0a209d0b814f216e0173b243f5217CAS | 7317343PubMed |

Tarrant PV (1981) The occurrence, causes and economic consequences of darkcutting in beef – a survey of current information. In ‘The problem of dark-cutting in beef’. (Eds DE Hood, PV Tarrant) pp. 25–62. (Martinus Nijhoff Publishers: Leiden, The Netherlands)

Tarrant PV (1988) Animal behaviour and environment in the dark-cutting condition. In ‘Dark cutting in cattle and sheep; proceedings of an Australian workshop’. (Eds SU Fabiansson, WR Shorthose, RD Warner) pp. 8–18. (Australian Meat and Livestock Research and Development Corporation: Sydney)

Tudor G, Coupar FJ, Pethick DW (1996) Effect of silage diets on glycogen concentration in the muscle of yearling cattle. Proceedings of the Australian Society of Animal Production 21, 451

Van den Top AM, Geelen MJH, Wensing T, Wentink GH, VantKlooster AT, Beynen AC (1996) Higher postpartum hepatic triacylglycerol concentrations in dairy cows with free rather than restricted access feed during the dry period are associated with lower activities of hepatic glycerolphosphate acyltransferase. The Journal of Nutrition 126, 76–85.

Vann RC, Burdick NC, Lyons JG, Welsh TH, Randel RD (2010) Influence of cattle temperament on stress hormones and IgG concentrations in Angus-cross calves. Journal of Dairy Science 93, 464–465.

Visek WJ (1984) Ammonia: its effects on biological systems, metabolic hormones, and reproduction. Journal of Dairy Science 67, 481–498.
Ammonia: its effects on biological systems, metabolic hormones, and reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhs12guro%3D&md5=d176700be2034bfa8a1a37fff3cbdfe2CAS | 6371080PubMed |

Voisinet BD, Grandin T, O’Connor SF, Tatum JD, Deesing MJ (1997) Bos indicus-cross feedlot cattle with excitable temperaments have tougher meat and a higher incidence of borderline dark cutters. Meat Science 46, 367–377.
Bos indicus-cross feedlot cattle with excitable temperaments have tougher meat and a higher incidence of borderline dark cutters.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MbnsVynsg%3D%3D&md5=89a7600a833a21f94e0800a6b3e04286CAS | 22062320PubMed |

Weekes TEC (1979) Carbohydrate metabolism. In ‘Digestive physiology and nutrition of ruminants’. (Ed. DC Church) pp. 187–209. (O & B Books Inc.: Corvallis, OR)

Wegner J, Albrecht E, Fiedler I, Teuscher F, Papstein H-J, Ender K (2000) Growth and breed related changes of muscle fibre characteristics in cattle. Journal of Animal Science 78, 1485–1496.

Wray-Cahen D, Dunshea FR, Boyd RD, Bell AW, Bauman DE (2012) Porcine somatotropin alters insulin response in growing pigs by reducing insulin sensitivity rather than changing responsiveness. Domestic Animal Endocrinology 43, 37–46.
Porcine somatotropin alters insulin response in growing pigs by reducing insulin sensitivity rather than changing responsiveness.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xkt1Cqs7k%3D&md5=2f724c7c3cb054100b23da282de61d45CAS | 22425435PubMed |